Ultrasonography as a Diagnostic Support Tool ... - JMA Journal

Original Research Article

Ultrasonography as a Diagnostic Support Tool for Childhood TakayasuArteritis Referred to as Fever of Unknown Origin: Case Series and LiteratureReview

Hisataka Nozawa1), Masao Ogura2), Mikiko Miyasaka3), Hiromichi Suzuki4), Kenji Ishikura2), Akira Ishiguro1), andShuichi Ito2),5)

Abstract:Introduction: Childhood Takayasu arteritis (c-TA) often shows nonspecific symptoms, such as fever of unknown origin(FUO). Delay of diagnosis may result in organ dysfunction by arterial occlusion; therefore, early diagnosis is very important.Although ultrasonography is the first-line screening tool for children with FUO, its diagnostic efficacy of evaluation of sys-temic arteries in c-TA that presents as FUO remains unclear. We evaluated the suitability of ultrasonography evaluation thatincluded systemic vessels for the early diagnosis of c-TA initially presenting as FUO.Methods: We review five patients who received a diagnosis of c-TA in our institution and also performed a literature reviewregarding TA cases with FUO and diagnosed on the basis of initial ultrasonography.Results: As in our cases, the median period from onset to diagnosis was 25 days (interquartile range [IQR], 21-35). Com-paring the initial ultrasonography findings with later contrast-enhanced computed tomography (CECT) findings in the ab-dominal aorta, celiac artery, superior mesenteric artery, bilateral renal arteries, and bilateral common carotid arteries, theconcordance rate between ultrasonography and CECT was moderate (Kappa coefficient was 0.50). All the patients weresuccessfully treated without severe vascular damage. The literature review revealed 12 articles; although 9 of the 13 patientsdid not show the characteristic features (such as blood pressure discrepancy, bruit, or pulse deficiency), the median time todiagnosis was still 5 months (IQR, 3-12).Conclusions: During initial screening for patients with FUO, ultrasonography including evaluation of systemic vesselscould contribute to earlier diagnosis of c-TA.

Key Words:Takayasu arteritis, pediatrics, diagnostic imaging, fever of unknown origin, ultrasonography

Introduction

Takayasu arteritis (TA) is a large vessel vasculitis affecting theaorta and its major branches. Childhood TA (c-TA) is a veryrare disease, with an annual incidence in the pediatric popula-tion of approximately 2/1,000,000 (1). Additionally, during theearly stages, its typical clinical manifestations (pulseless upperextremities, leg claudication, and fainting) are often lacking.Furthermore, c-TA often presents as a fever of unknown ori-gin (FUO). Kasai et al. reported that 4.8% of children withFUO eventually received a diagnosis of c-TA (2). Additionally,approximately 80% of patients with c-TA actually demonstrat-

ed fever (3), although that is a relatively minor symptom inadult TA (<34.7%) (4). Early diagnosis of c-TA is challengingfor pediatricians but is very important because delay in diag-nosis and intervention may result in vascular stenosis, dilation,and obstruction, which are often followed by organ dysfunc-tion.

The appropriate criteria from the American College ofRadiology state that ultrasonography may be appropriate forthe imaging modality evaluating pediatric patients withFUO (5) because it is free from radiation exposure and the needfor sedation. The recommendations from the European Lea-gue Against Rheumatism (EULAR) mention the early diag-

1) Center for Postgraduate Education and Training, National Center for Child Health and Development, Tokyo, Japan. 2) Division of Pediatric Nephrologyand Rheumatology, National Center for Child Health and Development, Tokyo, Japan. 3) Department of Radiology, National Center for Child Health andDevelopment, Tokyo, Japan. 4) Department of Health Policy, National Research Institute for Child Health and Development, Tokyo, Japan. 5) Department ofPediatrics, Graduate School of Medicine, Yokohama City University, Yokohama, JapanCorresponding author: Shuichi Ito, [email protected] J. 2021;4(4):358-366Received: December 16, 2020 / Accepted: June 2, 2021 / Advance Publication: September 13, 2021 / Published: October 15, 2021Copyright © Japan Medical Association

DOI: 10.31662/jmaj.2020-0115https://www.jmaj.jp/

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nosis by ultrasonography (6). However, the systematic review ofthe diagnosis of large vessel vasculitis states that there was nohigh-quality literature evaluating the usefulness of ultrasonog-raphy in the diagnosis of TA (7). If we could detect abnormalimaging findings of TA among patients with FUO with ultra-sonography screening, we would immediately select essentialradiological diagnostic procedures for definitive diagnosis ofTA, such as contrast-enhanced computed tomography(CECT). To the best of our knowledge, no literature has re-viewed the contribution of ultrasonography screening to thediagnosis of c-TA in patients with FUO. On the basis of theexperience of pediatric cases diagnosed as c-TA in patientswith FUO, we evaluated using case literature review the suita-bility of ultrasonography evaluation that included systemicvessels for the early diagnosis of c-TA initially presenting asFUO.

Materials and Methods

This study was performed in line with the principles of theDeclaration of Helsinki. Approval was granted by the EthicsCommittee of the National Center for Child Health and De-velopment on July 27, 2017 (number 1493), and written in-formed consent was obtained from all patients.

Patients and measurementsWe included all patients who were referred as FUO to the Na-tional Center for Child Health and Development in Tokyobetween March 2002 and March 2016 and who finally re-ceived a diagnosis of c-TA. Definitive diagnosis was based onEULAR, Paediatric Rheumatology International Trials Or-ganisation (PRINTO), and Paediatric Rheumatology Europe-an Society (PRES) criteria for TA (8). We excluded patientswho already had suspected c-TA by several radiological proce-dures performed in previous hospitals and were referred fortreatment of c-TA. We investigated their clinical findings, in-cluding sex, age of onset, laboratory examinations (C-reactiveprotein level and erythrocyte sedimentation rate), durationfrom onset to diagnosis, Indian Takayasu Activity Score 2010(ITAS2010) at diagnosis and at the latest ultrasonography fol-low-up date until July 2020, treatment, and Vasculitis Dam-age Index (VDI) at the latest ultrasonography follow-up dateuntil July 2020.

We also compared the ultrasonography and CECT find-ings of our patients regarding the following seven vessels: ab-dominal aorta (AAo), celiac artery, superior mesenteric artery(SMA), right and left renal arteries, and right and left com-mon carotid arteries (CCAs).

Search strategy and study selectionWe searched PubMed, Ovid/MEDLINE, Embase, and Co-chrane library databases for previously published studies untilAugust 31, 2020. In each database, the search query was thefollowing: (“Takayasu arteritis”[MeSH Terms] OR “takaya-

su*”[Title/Abstract]) AND (“ultrasonography”[MeSHTerms] OR (“ultrasound”[Title/Abstract] OR “ultrasonogra-phy”[Title/Abstract] OR “sonography”[Title/Abstract])) inPubMed and Ovid/MEDLINE and (‘aortic archsyndrome’/exp OR ‘takayasu*’:ab,ti) AND (‘echography’/expOR ‘ultrasound’:ab,ti OR ‘ultrasonography’:ab,ti OR ‘sonog-raphy’:ab,ti) AND [english]/lim AND [embase]/lim in Em-base, ([Takayasu Arteritis] explode all trees) AND ([Ultraso-nography] explode all trees) in Cochrane library. English lan-guage filter was activated in PubMed and Ovid/MEDLINE.We also performed a manual search of reference literaturefrom the full text available studies.

Case reports about the diagnosis of TA by the initial ultra-sonography for patients with FUO were included. Review ar-ticles and the literature lacking the correct clinical course forindividual patients were excluded.

Results

Characteristics and clinical manifestations ofenrolled patientsDuring this study period, five patients received a diagnosis ofc-TA. Table 1 shows the summary of the five patients. All pa-tients had suspected TA by the initial screening ultrasonogra-phy and then received a definitive diagnosis on the follow-upCECT. They fulfilled the EULAR-PRINTO-PRES diagnos-tic criteria. The median age at onset was 11 years (interquartilerange [IQR], 9-12 years). The median duration from onset todiagnosis was 25 days (IQR, 21-35 days). The median value ofITAS2010 at diagnosis was 3 (IQR, 1-9). All patients receivedimmunosuppressive treatment, and the value of ITAS2010decreased to 0 at the most recent ultrasonography follow-update. The highest value of VDI among five patients was 2.

Ultrasonography and CECT findingsTable 2 shows the radiological findings of ultrasonographyand CECT for seven arteries. Figure 1 (panels a, b, c, d, e, andf) shows the representative ultrasonograms. All findings wereclassified as follows: 9 arteries were positive on both ultraso-nography and CECT (6 abdominal and 3 cervical), 2 werepositive on ultrasonography alone (1 abdominal and 1 cervi-cal), 6 were positive on CECT alone (4 abdominal and 2 cervi-cal), and 16 were negative on both ultrasonography andCECT (14 abdominal and 2 cervical). For patient 5, bilateralCCAs were not evaluated by either ultrasonography orCECT. There was moderate agreement between ultrasonogra-phy and CECT assessment on all arteries and abdominal arter-ies (Kappa coefficients were 0.50 and 0.56).

Study reviewAccording to the search strategy, inclusion and exclusion crite-ria, 12 articles including 13 cases were re-viewed (9), (10), (11), (12), (13), (14), (15), (16), (17), (18), (19), (20). Figure 2 shows aflowchart depicting the article screening and selection.

DOI: 10.31662/jmaj.2020-0115JMA Journal: Volume 4, Issue 4 https://www.jmaj.jp/

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Table 3 shows the summary of all patients in the reviewed ar-ticles. Only three of 13 patients showed specific manifesta-tions, including bruit, pulse deficit, or blood pressure discrep-ancy. The median duration from onset to diagnosis was 5months (IQR, 3-12 months).

Discussion

According to the present study, it is important for early diag-nosis of c-TA to perform ultrasonography screening that in-cludes large systemic vessels (as many as we can observe)among children with FUO. Detection of ultrasonography ab-normalities may lead to confirmative examinations, such as viaCECT, and early diagnosis of c-TA contributed to favorablepatient outcomes. The diagnosis of TA is generally made by acombination of imaging modalities. Our study showed that

ultrasonography was able to detect abnormal arteries in theabdomen and neck regions with a moderate concordance ratecompared with CECT. In the early stage of TA, patients showonly nonspecific symptoms, such as persistent fever. Addi-tionally, in the so-called “pre-pulseless phase” of vascularstenosis, pulse deficit or blood pressure discrepancy, which arehallmarks of TA, may be lacking (21). However, both in our pa-tients and in cases from the review articles, the median dura-tion from onset to definitive diagnosis tends to be shorter thanthose stated in the previous studies (22), (23), (24), (25). Furthermore,ultrasonography is minimally invasive (free from radiation ex-posure or sedation) and low in cost and provides satisfactoryaccess to images. Thus, it is preferable as a screening and diag-nostic support tool for c-TA among children with FUO.

There are two reasons why ultrasonography evaluation ofsystemic arteries, particularly including those in the abdomen,

Table 1. Summary of Clinical Manifestations of Five Patients.

CaseNo.

Sex/Age atonset

Clinicalsymptomsother than

fever

Applicablenumber to

EULAR-PRINTO-

PREScriteria/presenceof bruit

Laboratorydata at

diagnosisDuration

fromonset to

diagnosis(days)

ITAS2010at

diagnosis

Treatment Follow-up status at mostrecent US date

CRP(mg/dL)

ESR(mm/

h)

Inductiontherapy

Presenttherapy ITAS2010 VDI

Follow-up period(months)

1 F/12years

Knee pain 3/Yes 7.8 129 25 9 MPT PSL/AZP/MTX

0 1 53

2 M/9years

Abdominal pain 1/No 8.2 132 21 1 MPT PSL/AZP 0 1 55

3 M/12years

Abdominal pain 2/Yes 10.4 106 15 3 MPT/IVCY MMF 0 2 70

4 F/11years

Lymphadenopathy 4/Yes 3.0 113 35 11 MPT/IVCY None 0 1 91

5 F/5months

Cough 2/No 11.5 132 37 0 MPT/IVCY None 0 0 60

AZP, azathioprine; CRP, C-reactive protein; ESR, erythrocyte sedimentation rate; EULAR, European League Against Rheumatism; F, female; IVCY, intravenouscyclophosphamide therapy; ITAS, Indian Takayasu activity score, M, male; MMF, mycophenolate mofetil; MPT, methylprednisolone pulse therapy; MTX, methotrexate;PRES, Pediatric Rheumatology European Society; PRINTO, Pediatric Rheumatology International Trials Organization; PSL, prednisolone; VDI, vasculitis damage index

Table 2. Arterial Findings Compared between Ultrasonography and Contrast-enhanced Computed Tomography.

Case No.Abdominal arteries (US/CECT) Cervical arteries (US/CECT) US undetectable lesions

detected by CECTAAo CA Right RA Left RA SMA Right CCA Left CCA

1 −/＋ −/− −/＋ −/− ＋/＋ −/− ＋/＋ Wall thickening of the leftsubclavian artery and trunk of right

renal artery

2 −/－ −/− −/− −/− −/− −/＋＋/＋ None

3 −/− ＋/＋ −/− −/− ＋/＋ −/− ＋/＋ None

4 −/＋ −/＋ −/− −/− ＋/＋＋/− −/＋ None

5 ＋/＋＋/＋ −/− −/− ＋/− NA NA None

AAo, abdominal aorta; CA, celiac artery; CCA, common carotid artery; CECT, contrast-enhanced computed tomography; NA, not available; RA, renal artery; SMA,superior mesenteric artery; US, ultrasonography


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is suitable for c-TA patients among children with FUO: first,different distribution of arterial involvement in c-TA com-

pared with that in adult TA and, second, favorable body habi-tus of children for ultrasonography screening.

Figure 1. Representative images of arterial involvement comparing ultrasonography with contrast-enhanced computed tomogra-phy (CECT) in Patient No. 3 (panels a, b, c, d, e, and f).a: Transverse view shows wall thickening at the level of the trunk of the superior mesenteric artery (SMA) in the ultrasonogram(arrow).b: CECT at the same level of the abdominal ultrasonogram demonstrates wall thickening of the SMA (arrow).c: Longitudinal view shows arterial stenosis at the level of the trunk of the celiac artery (CA), and wall thickening of the SMA inthe ultrasonogram (arrow).d: CECT at the same level of the abdominal ultrasonogram recognizes both findings of the CA and SMA (arrow).e: Wall thickening of the left common carotid artery (CCA) is shown in the transverse view in the ultrasonogram (arrow).f: Wall thickening of the left CCA is revealed by CECT at the same level of the neck ultrasonogram (arrow).AAo, abdominal aorta; CA, celiac artery; CCA, common carotid artery; Lt., left; SMA, superior mesenteric artery.


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Recent reports revealed that c-TA is more likely to demon-strate subphrenic aorta involvement rather than in intrathora-cic or suprathoracic regions (26), (27), (28). Our results were alsoconsistent with this presentation. A retrospective cohort studyof c-TA in the United States reported that the frequency ofabdominal involvement was 52.4% in the AAo and 42.9% inthe SMA, and (in the thorax and neck) 38.1% in the rightCCA and 42.9% in the left CCA (29). Feng et al. reported arteri-al involvement in 11 patients with c-TA. All 11 patients hadinvolvement of the AAo and its branches, but only three(27.2%) had involvement of the CCAs (30).

As mentioned above, the body habitus of children is fa-vorable for abdominal ultrasonography screening comparedwith that of adults. They have a thinner abdominal wall andless fat compared with adults (31), thus enabling higher-resolu-tion ultrasonography images. The “macaroni sign,” which is along, smooth, homogeneous, and moderately echogenic cir-cumferential thickening of the cervical arteries on the trans-verse section, specific for early TA (32), (33), (34), is similarly ob-served in the abdominal region in our patients. In adults, ab-dominal arteries are often obscured because ultrasonographycannot visualize them because of a larger physique with thicksubcutaneous tissue or large volumes of bowel gas. Thus, inadult TA, the efficacy of ultrasonography is mainly limited to

CCAs (35), (36), (37). Among the cases in the review articles, the pa-tients’ median age whose involvement of the abdominal arter-ies could be detected by ultrasonography was 20 years (range,12-54 years), which tended to be young.

Ultrasonography findings did not completely correspondwith CECT findings in the cervical regions. The Kappa coeffi-cient, which indicates the concordance rate between ultraso-nography and CECT, also tended to be slightly higher in theabdominal region only than in the abdominal and cervical re-gions together. It may suggest that cervical CECT may be in-ferior to abdominal CECT in diagnostic accuracy. As subcu-taneous fat and tissue during childhood are significantly thin-ner in the neck area than in adults, it is difficult to distinguishthe arterial wall from the periarterial soft tissue in CECT. Ad-ditionally, technical problems, such as motion artifact or inac-curate scan setting (timing and slice thickness), can affect im-age quality. These also apply to magnetic resonance imaging(MRI) and may be a common caveat particularly in childrenwho are small and difficult to immobilize for a long time. Fur-thermore, if the arterial abnormality (i.e., wall thickening) islocalized in a small section of the carotid artery, as shown inFigure 3 (panels g, h, and i), CECT may not differentiatesuch small vascular abnormalities. As CECT or MRI is not al-ways a definitive imaging modality, additional ultrasonogra-

Figure 2. Flowchart of the literature review on Takayasu arteritis diagnosed with ultrasonography among patients with fever ofunknown origin.


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phy examination should be considered when c-TA is suspect-ed.

Although the results of our study encourage initial ultra-sonography screening of systemic arteries to find c-TA in chil-dren with FUO, our study has several limitations. First, thisstudy was a retrospective analysis with small numbers of pa-tients at a single center. Second, TA is a more well-known andprevalent disease among Japanese and other Asian popula-tions than among those of Europe and the United States.Third, ultrasonography is dependent on observers’ skills andcannot visualize the proximal subclavian artery and thoracicaorta because of the interference of the costal bones and the

normal presence of air in the lung. Finally, we compared onlyultrasonography and CECT but did not include contrast-en-hanced ultrasonography (CEUS) or MRI. Recently, CEUSand MRI have been added as effective tools for the diagnosisand assessment of disease activity in TA (32), (37), (38), (39). CEUS hasnot yet been introduced in our institution. When screeningfor FUO, we performed CECT as a secondary survey prior toMRI to search for fever sources other than arteritis. Consider-ing that some patients at the susceptible age for TA do not al-ways require sedation during short-term MRI, in the future,we intend to perform MRI focusing on abnormal arteries toconfirm the diagnosis of TA.

Table 3. Summary of Literature Review on TA Cases Detected by Initial US Screening among Patients with Fever of UnknownOrigin.

Study

Sex/Age at

onset(years)

Clinicalsymptoms

otherthan fever

Applicablenumber

to EULAR-PRINTO-

PREScriteria/Presenceof a bruit

Laboratorydata at

diagnosisDuration

fromonset to

diagnosis(months)

US/Definitive imageModality

fordefinitivediagnosis

Follow-up

period(months)

Presenttherapy Relapse

CRP(mg/d

L)

ESR(mm/

h)Abdominal Cervical/

Thoracic

Tachibanaet al

F/20 Painthroughoutentire body

1/No 7.5 99 4 NA/+ +/+ CTA 6 PSL/MTX

Yes

Goel et al M/18 Dyspnea 1/No 6.0 35 6 +/+ +/+ CTA 3 PSL/MTX

No

Sasae et al F/20 Periumbilicalpain

2/No 9.1 119 3 +/+ +/+ CTA 4 PSL No

Sada et al F/19 Malaise 1/No 31.2 145 6 NA/NA +/+ CTA 24 PSL/MTX

No

Agostiniset al

M/75 Cough andneck pain

1/No 15.1 85 3 NA/+ +/+ FDG-PET 6 PSL/MTX

No

Gupta etal

F/20 Painfulnodular skin

lesions

2/No 15.2 77 12 +/+ NA/+ MRA NA PSL No

Ahasan etal

F/20 Pain in allfour limbs

2/No 1.2 62 2 +/NA NA/NA NA NA PSL NA

Thai et al F/14 Pain in leftupper

extremity

4/Yes 21000.0 154 4 NA/NA +/NA MRA NA PSL NA

Skoura etal

F/54 None 1/No 2.0 80 NA +/NA NA/+ FDG-PET 6 PSL NA

Uthmanet al

F/28 None 1/No NA 150 18 NA/NA +/+ DSA 5 PSL/MTX

NA

KiŞlaEkİncİ etal

F/12 Painful lesionon the face

1/No 14.8 116 2 +/+ +/+ MRA 18 PSL/MTX/MM F

Yes

Schmidtet al

F/38 Joint pain 1/No 3.6 92 12 NA/NA +/+ DSA 14 PSL/AZP No

F/27 Joint pain 1/No 24.6 120 36 NA/NA +/+ DSA 8 PSL/MTX

Yes

AZP, azathioprine; CTA, computed tomography angiography; CRP, C-reactive protein; DSA, digital subtraction angiography; ESR, erythrocyte sedimentation rate;EULAR, European League Against Rheumatism; F, female; FDG-PET, [18F]-fluorodeoxyglucose positron emission tomography; M, male; MMF, mycophenolatemofetil; MRA, magnetic resonance angiography; MTX, methotrexate; NA, not available; PRES, Pediatric Rheumatology European Society; PRINTO, PediatricRheumatology International Trials Organization; PSL, prednisolone; US, ultrasonography


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ConclusionUltrasonography is preferable as a screening and diagnosticsupport tool for c-TA referred to as pediatric patients withFUO. For early diagnosis of c-TA, it is important to performultrasonography screening that includes large systemic vessels(as many as we can observe) among children with FUO.

Article Information

Conflicts of InterestShuichi Ito has the following conflicts of interest relevant tothis article to disclose: an advisory fee from Takeda Pharma-ceutical, and the lecture fees from Chugai Pharmaceutical,Mitsubishi Tanabe Pharma, Pfizer, and Takeda Pharmaceuti-cal, and research funding from Chugai Pharmaceutical andMitsubishi Tanabe Pharma.

Kenji Ishikura has the following conflicts of interest rele-vant to this article to disclose: honoraria from Asahi KaseiPharma, Chugai Pharmaceutical, Novartis Pharma, and Zen-yaku Kogyo, and research funding from Chugai Pharmaceuti-cal and Zenyaku Kogyo.

AcknowledgementWe thank the medical editor from the Division of Education

for Clinical Research, National Center for Child Health andDevelopment for editing this article.

Author ContributionsAll authors contributed to the conception and design of thestudy. Hisataka Nozawa provided material preparation, datacollection, interpretation, and participated in the design, andrevision of the review and wrote the first draft of the manu-script. Mikiko Miyasaka revised figures and figure legends.Hiromichi Suzuki developed the search strategy for searches.Shuichi Ito supervised the entire process. All authors com-mented on previous versions of the manuscript, approved thefinal manuscript as submitted, and agreed to be accountablefor all aspects of the work.

DisclaimerShuichi Ito is one of the Editors of JMA Journal and on thejournal’s Editorial Staff. He was not involved in the editorialevaluation or decision to accept this article for publication atall.

Approval by Institutional Review Board (IRB)This study was performed in line with the principles of theDeclaration of Helsinki. Informed consent was obtained from

Figure 3. Transverse imaging of bilateral CCAs in Patient No. 4 (panels g to i).g and h: Thickening at the dorsal walls of bilateral CCAs is clearly detected via ultrasonography (panel g shows the right side, andpanel h shows the left side).i: Wall thickening at the same level is unclear in CECT.CCA, common carotid artery; IJV, internal jugular vein; T, thyroid gland.


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all individual participants included in this study and their pa-rents. The participants and their parents consented to the sub-mission of the case series to the journal. Approval was grantedby the Ethics Committee of the National Center for ChildHealth and Development on July 27, 2017 (number 1493).

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